sign in sign up
<<
Home , Matsucoccidae, Pinus strobus

FOREST ENTOMOLOGY Matsucoccus macrocicatrices (: Matsucoccidae): First Report, Distribution, and Association With Symptomatic Eastern White in the Southeastern United States

ANGELA M. MECH,1,2 CHRISTOPHER ASARO,3 MICHELLE M. CRAM,4 DAVID R. COYLE,1 5 6 1 PENELOPE J. GULLAN, LYN G. COOK, AND KAMAL J. K. GANDHI

J. Econ. Entomol. 106(6): 2391Ð2398 (2013); DOI: http://dx.doi.org/10.1603/EC13251 ABSTRACT We provide the Þrst report of Matsucoccus macrocicatrices Richards (Hemiptera: Mat- sucoccidae) feeding and reproducing on eastern white pine, L., in the southeastern United States. Until now, M. macrocicatrices had been reported only from the Canadian Atlantic Maritimes, , and . Entomological holdings of 27 major museums in eastern have no historical records for M. macrocicatrices from the southeastern region. However, our Þeld surveys and molecular analyses (DNA barcoding) have resulted in the collection and positive identiÞcation of M. macrocicatrices in , , , , , and . In addition to the new geographic range, M. macrocicatrices is also being associated with dieback and mortality of all diameter classes of P. strobus leading to concern about a potential shift from its historically nonpestiferous presence on the host . On P. strobus, M. macrocicatrices was found embedded in cankers or present on top of the bark with necrotic tissue under their feeding area, indicating that they may be creating wounds for opportunistic pathogenic fungi to infest. Further, we found M. macrocicatrices living outside of the epiphytic mats of its symbiotic fungus, Septobasidium pinicola Snell. This study shows that M. macrocicatrices is now widespread in the southeastern United States, with implications for the future survival and regeneration of P. strobus in eastern North America.

KEY WORDS eastern white pine, Matsucoccidae, Matsucoccus macrocicatrices, Pinus strobus, south- eastern United States

The genus Matsucoccus Cockerell, commonly known recently been synonymized (Morrison 1939, Parr as the pine bast scales or matsucoccids (Hemiptera: 1939, Richards 1960, Watson et al. 1960, Ray and Wil- Coccoidea: Matsucoccidae), is a group of widely dis- liams 1991, Kosztarab 1996, Booth and Gullan 2006; tributed scale in temperate, tropical, and sub- Table 1). Among these scale species, M. gallicolus has tropical areas of the world. There are 32 extant Mat- the widest native host and distribution range in east- sucoccus species worldwide, with 19 in North America ern North America. M. alabamae is reported only from that all feed exclusively on in the family pine trees in ; M. banksianae from jack pine (BenÐDov 2005, 2012). Eastern North American for- (Pinus banksiana Lambert) in ; M. macro- ests have Þve species of Matsucoccus: 1) Matsucoccus cicatrices from eastern white pine (Pinus strobus L.) in alabamae Morrison; 2) Matsucoccus banksianae Ray the Canadian Maritime Provinces, New Hampshire, and Williams; 3) Matsucoccus gallicolus Morrison; 4) and Massachusetts; and M. matsumurae from red pine Matsucoccus macrocicatrices Richards; and 5) Matsu- (Pinus resinosa Aiton) in , Massachusetts, coccus matsumurae (Kuwana), a nonnative species for New Hampshire, , , Pennsylva- which Matsucoccus resinosae Bean and Godwin has nia, and (Table 1). Several Matsucoccus species are known to be pes- 1 Daniel B. Warnell School of and Natural Resources, tiferous and economically important, as their feeding University of Georgia, 180 East Green St., Athens, GA 30602. activities have been implicated in dieback and mor- 2 Corresponding author, e-mail: [email protected]. tality of both mature and young pine trees. For ex- 3 Virginia Department of Forestry, 900 Natural Resources Drive, ample, in the southwestern United States, the pinyon Suite 800, Charlottesville, VA 22903. 4 USDA Forest Service, Forest Health Protection, 320 Green St., needle scale, Matsucoccus acalyptus Herbert, can cause Athens, GA 30602. defoliation and mortality of pinyon pine (Pinus edulis 5 Division of Evolution, Ecology and Genetics, The Research Engelmann) after repeated feeding (McCambridge School of Biology, The Australian National University, Canberra, ACT and Pierce 1964). The nonnative M. matsumurae was 0200, Australia. 6 School of Biological Sciences, The University of Queensland, responsible for foliage discoloration (Bean and God- Brisbane, QLD 4072, Australia. win 1955) and mortality of -grown P. res- 2392 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 6

Table 1. Pine hosts and collection localities of Matsucoccus scale species documented in eastern North America

Collection locality in eastern North Scale species Pine hosts in eastern North America Citations America M. alabamae Pinus spp. Alabama Morrison (1939), Drooz (1985) Morrison M. banksianae P. banksiana Lambert Minnesota Ray and Williams (1991) Ray & Williams M. gallicolus P. echinata Miller, P. elliottii Connecticut, District of Columbia, , Morrison (1939), Parr (1939), Morrison Engelm., P. glabra Walter, Georgia, , Massachusetts, Drooz (1985), Kosztarab P. ponderosa Douglas ex Lawson, , , , North (1996) P. pungens Lambert, P. resinosa Carolina, New Hampshire, New Jersey, Aiton, P. rigida Miller, P. serotina New York, , , Rhode Michaux, P. taeda L., P. virginiana Island, Tennessee, Virginia Miller M. macrocicatrices P. strobus L. Massachusetts, New Brunswick, New Richards (1960), Watson et al. Richards Hampshire, Nova Scotia, , (1960), Martineau (1964), Drooz (1985), Kosztarab (1996), Foldi (2004) M. matsumurae P. densiflora Siebold & Zuccarinia, Connecticut, Massachusetts, New Bean and Godwin (1955, 1971), (Kuwana) P. resinosa, P. rigida, P. Hampshire, New Jersey, New York, Drooz (1985), Kosztarab tabulaeformis Carrie`rea, P. Pennsylvania, Rhode Island (1996), Li and Zhao (1997), thunbergii Parlatorea New Hampshire Division of Forests and Lands (2012), USDA Forest Service, Forest Health Protection (2013)

a Asian pine species. inosa in Connecticut (McClure 1983). M. gallicolus a number of vertebrate wildlife species for food, pro- was responsible for killing terminal leaders on Ͼ63% tection, and shelter (Wendel and Smith 1990). In of pitch pine (Pinus rigida Miller) trees in Pennsyl- addition, P. strobus is commercially valuable as both a vania, and caused Ͼ50% mortality in pitch pine stands timber and species in the United States in Massachusetts (Parr 1939). (Wendel and Smith 1990). In the northeastern region Recently, eastern white pine (P. strobus) trees in of the United States, P. strobus is one of the most mixed and pure stands started showing dieback in the harvested species and is listed as having the of Virginia (2006) and Geor- highest volume of sawtimber in four states (Maine, gia (2011). Symptoms included branch ßagging, Massachusetts, New Hampshire, and Rhode Island; crown thinning, resinosis at branch crotches and on Butler et al. 2012a,b; McCaskill and McWilliams 2012; the main stem, and cankers on all diameter classes of Morin and Woodall 2012). trees. Follow-up visits to several locations revealed an Similar to Georgia and Virginia, dieback and mor- increase in the number of symptomatic trees as well as tality of P. strobus has also been reported in Maine, tree mortality. On close inspection of branches and New Hampshire, Ontario, and West Virginia, and has main stems, small black immature stages of a scale been attributed largely to pathogens such as Calici- were found embedded in the majority of the opsis pinea Peck (Lombard 2003, Maine Forest Service cankers, under lichen, and in branch crotches (Fig. 1A 2008, 2011, Llewellyn 2013). Examination of and B). In 2007, scale specimens from Bath County, symptomatic P. strobus samples from New Hampshire VA, were sent to the Florida Department of Agricul- and West Virginia revealed immature insects of a Mat- ture and Consumer Services where they were tenta- tively identiÞed as an immature instar of a Matsucoccus sucoccus species embedded in the majority of the can- species based on morphological characteristics (G. kers, including the C. pinea cankers. A cursory exam- Hodges, personal communication). The of ination of the fungi associated with cankers and Matsucoccus is based on adult females and immature feeding scales of Matsucoccus on P. strobus in Virginia cyst-stage specimens cannot be identiÞed to species revealed the presence of a number of common, op- based on morphology. The only known Matsucoccus portunistic, typically nonaggressive fungal pathogens scale to use P. strobus as a host is M. macrocicatrices, but including C. pinea, Diplodia scrobiculata de Wet, Slip- this species has never been documented as being as- pers & WingÞeld, Fusarium chlamydosporium Wol- sociated with severe dieback or mortality of the host lenw. & Reinking, and Fusarium acuminatum Ellis & tree, nor has it been reported south of Massachusetts. Everh. (Cram et al. 2009). P. strobus is a long-lived, ecologically and econom- Our research objectives were to: 1) identify the ically important conifer species in North America with Matsucoccus species present on symptomatic P. stro- a native range encompassing 31 states and provinces bus; 2) determine the geographic distribution of this (Fig. 2). It is a dominant or codominant tree in 30 Matsucoccus species in the southeastern United States; Society of American Foresters forest cover types, has and 3) conduct a cursory examination of the fungi been planted to aid in soil reclamation, and is used by associated with symptomatic trees of P. strobus in December 2013 MECH ET AL.: REPORT OF M. macrocicatrices IN SOUTHEASTERN U.S. 2393

Fig. 1. M. macrocicatrices (from Georgia): (A and B) Overwintering cyst stage embedded in cankers. (C) Emerging adult. (D) Necrotic tissue under feeding sites. Arrows indicate M. macrocicatrices individuals (A and B) or feeding sites (D). (Online Þgure in color.)

Georgia, including the tissue found with feeding Mat- template. PCR of both 18S and 28S used an initial step sucoccus scales. of denaturation at 94ЊC for 4 min, followed by 35 cycles of denaturation at 94ЊC for 30 s, primer annealing at 55ЊC for 30 s and primer extension at 72ЊC for 1 min, Materials and Methods and completed with a Þnal elongation step of 72ЊC for Matsucoccus Identification. In January, 2012, col- 3 min. PCR products were treated with Exonuclease lections of immature scale insects from the Chatta- I and Antarctic Phosphatase (New England Biolabs, hoochee National Forest (Habersham County), GA, Queensland, Australia) before sending to Macrogen were stored in 90% EtOH and sent to The Australian Inc. (Republic of Korea). National University (ANU) and The University of Sequences were edited using Geneious R6 (Biom- Queensland (UQ), Australia, for identiÞcation using atters 2012) and aligned manually in Se-Al (Rambaut DNA sequence analysis. DNA was extracted nonde- 2002). Nexus Þles were imported into Geneious R6 structively from individual specimens and ampliÞed and analyzed using Neighbor-Joining clustering for nuclear rDNA genes (18S and 28S), which have method with the Tamura Nei algorithm implemented been shown to be useful in identifying species of in Geneious R6. One thousand bootstrap pseudo-rep- Matsucoccus (Booth and Gullan 2006). An Ϸ600 bp licates were conducted using the same program to fragment of 18S was ampliÞed using primers 2880 and assess node support. B- (Von Dohlen and Moran 1995), and the D2ÐD3 In May 2012, adult females were found in Murray domains of 28S (Ϸ750 bp) were ampliÞed with S3360 County, GA, and were sent to the ANU for species (Dowton and Austin 1998) and A335 (Whiting et al. identiÞcation based on adult female morphology. 1997). Polymerase chain reaction (PCR) was carried These specimens are housed in the Australian Na- ␮ ␮ ␮ out in 25 l volumes that included 13 lH2O, 5 l tional Insect Collection, Commonwealth ScientiÞc MangoTaq 5ϫ PCR buffer (Bioline, Sydney, Austra- and Industrial Research Organization Ecosystem Sci- ␮ ␮ ␮ lia), 2 l dNTP (2 mM), 1.5 l MgCl2 (50 mM), 0.5 l ences, Canberra, Australia. of each of the forward and reverse primers (each at 10 Matsucoccus Distribution. In late 2012 and early ␮M),1UofMangoTaq (Bioline), and 2 ␮lofDNA 2013, sampling for Matsucoccus on P. strobus was ex- 2394 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 6

Fig. 2. M. macrocicatrices distribution map by state and province in eastern North America. Inset map shows collection locations in the southeastern United States as of January 2013. Note that the entire states or provinces were colored to indicate the presence of M. macrocicatrices, and that this does not indicate that M. macrocicatrices is present everywhere in that particular state or province. (Online Þgure in color.) panded to other states in the southeastern region of known symptomatic stands, whereas P. strobus sam- the United States. Branches of P. strobus from Georgia, ples from Kentucky, North Carolina, South Carolina, Virginia, and West Virginia were collected from and Tennessee were randomly collected based on December 2013 MECH ET AL.: REPORT OF M. macrocicatrices IN SOUTHEASTERN U.S. 2395

Table 2. Collection information for M. macrocicatrices on P. strobus in the southeastern United States (locations refer to Fig. 2)

State County Latitude and longitude Collection date Georgia Gilmer 34Њ43Ј21.179Љ, Ϫ84Њ12Ј16.308Љ 20 Nov. 2012 Habersham 34Њ45Ј24.048Љ, Ϫ83Њ35Ј01.967Љ 18 Dec. 2011 Lumpkin 34Њ41Ј44.448Љ, Ϫ83Њ57Ј01.511Љ 28 Sept. 2012 Murray 34Њ52Ј20.711Љ, Ϫ84Њ39Ј00.144Љ 18 April 2012 Rabun 34Њ50Ј31.415Љ, Ϫ83Њ25Ј25.752Љ 4 Jan. 2013 Stephens 34Њ40Ј17.652Љ, Ϫ83Њ21Ј36.072Љ 18 Nov. 2012 Townes 34Њ51Ј04.212Љ, Ϫ83Њ47Ј42.648Љ 28 Sept. 2012 White 34Њ47Ј56.471Љ, Ϫ83Њ44Ј42.251Љ 28 Sept. 2012 North Carolina Jackson 35Њ07Ј02.532Љ, Ϫ83Њ00Ј43.487Љ 4 Jan. 2013 Jackson 35Њ06Ј47.052Љ, Ϫ83Њ06Ј44.171Љ 4 Jan. 2013 Macon 35Њ02Ј14.460Љ, Ϫ83Њ15Ј26.928Љ 4 Jan. 2013 Macon 35Њ04Ј58.908Љ, Ϫ83Њ11Ј19.212Љ 4 Jan. 2013 Madison 35Њ49Ј18.768Љ, Ϫ82Њ31Ј42.672Љ 9 Jan. 2013 Transylvania 35Њ07Ј34.175Љ, Ϫ82Њ54.56.123Љ 4 Jan. 2013 South Carolina Greenville 35Њ04Ј15.312Љ, Ϫ82Њ38Ј41.531Љ 11 Dec. 2012 Oconee 34Њ50Ј34.907Љ, Ϫ83Њ07Ј50.627Љ 11 Dec. 2012 Tennessee Unicoi 36Њ03Ј11.951Љ, Ϫ82Њ31Ј51.671Љ 9 Jan. 2013 Virginia Bath 38Њ01Ј53.652Љ, Ϫ79Њ51Ј27.216Љ 20 July 2011 Highland 38Њ17Ј59.999Љ, Ϫ79Њ24Ј29.998Љ 28 Nov. 2012 West Virginia Hardy 39Њ04Ј14.268Љ, Ϫ78Њ34Ј41.051Љ 22 Oct. 2012 Monroe 37Њ37Ј07.895Љ, Ϫ80Њ14Ј19.464Љ 15 Oct. 2012 road surveying for trees. In total, 31 locations in 25 1983), pine needle agar (PNA; Blodgett et al. 2003), counties were sampled with two or more counties per and potato dextrose agar with streptomycin and teri- state. Branches were examined for the presence of the gitol (PDAϩSϩT) medium (Steiner and Watson immature cyst stages that were collected (n ϭϷ15 per 1965). Plated samples were incubated at 20ЊC for 4 wk location), and sent to UQ for identiÞcation. All im- with weekly observations for identiÞcation or transfer mature cyst stages were stored in 90% EtOH and of isolates to fresh media. UnidentiÞable mycelium DNA-barcoded as described previously for species isolates that did not produce spores on the initial determination. A reference collection of remaining medium used were transferred to carnationÐleaf water immature cyst stages and adults not sent to UQ are agar medium (Nelson et al. 1983) or to PNA in an deposited at the Georgia Museum of Natural History, attempt to induce spore production for identiÞcation. University of Georgia, Athens. In addition to Þeld These second transfers were also observed weekly for surveys, entomological holdings of 27 major museums 4 wk. in eastern North America were searched for Matsu- coccus specimens to determine whether any historical records of this insect existed that were not recorded Results in the literature. Fungus Identification. From March to August of Matsucoccus Identification. Molecular analysis 2012, in total, 120 branches (10 branches collected matched the specimens collected in 2012 and 2013 to biweekly) were collected from individual symptom- M. macrocicatrices. The sequences of the 18S and 28S atic P. strobus trees in Habersham County, GA, to be D2ÐD3 gene regions from all collections were identi- examined for the occurrence of C. pinea or of Septo- cal to those of M. macrocicatrices previously collected basidium pinicola Snell, an epiphytic fungus known to and identiÞed from Massachusetts, with strong boot- be mutualistic with some sap-sucking insects, includ- strap support (92% for 18S and 100% for the 28S D2ÐD3 ing Matsucoccus (Couch 1938, Watson et al. 1960). region). Genbank accession numbers for the 28S IdentiÞcations of these fungi were based on the sper- D2ÐD3 and 18S regions are KF040554ÐKF040572 and magonia and ascocarp fruiting structures of C. pinea KF053072ÐKF053091, respectively. Furthermore, the (Benny et al. 1985) and the diagnostic fungal mat of S. identity of adult females from Murray County, GA, pinicola (Couch 1938). was conÞrmed as M. macrocicatrices based on pub- Additional branches from individual P. strobus trees lished adult morphology (Richards 1960). in Habersham County, GA, were collected to identify Matsucoccus Distribution. Of the 25 counties sam- fungi occurring in the necrotic tissue surround- pled, 19 (76%) contained P. strobus with M. macroci- ing individuals of Matsucoccus not associated with can- catrices (Fig. 2; Table 2). The six county samples lack- kers. In total, 72 scales (maximum six per branch) were ing M. macrocicatrices were all collected from removed from the host anda5by5mm2 area of the nonsymptomatic, randomly selected P. strobus. Re- P. strobus tissue that surrounded each scale was placed sults indicate that M. macrocicatrices is now present on in 10% bleach at 6% active ingredient for 40 s. The P. strobus in Georgia, North Carolina, South Carolina, surface-sterilized tissue was then washed in sterile Tennessee, Virginia, and West Virginia (Fig. 2; Table water for 1 min and blotted dry with sterile paper 2). The survey of entomological holdings of 27 muse- towels. Samples were divided evenly on three types of ums in eastern North America resulted in no historical media: modiÞed NashÐSnyder medium (Nelson et al. records of M. macrocicatrices from the southeastern 2396 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 6

Table 3. Reports of M. macrocicatrices in museum collections in eastern North America

State or province Institution Holdings Alabama Auburn University No M. macrocicatrices in collection Connecticut University of Connecticut No M. macrocicatrices in collection Florida Florida Department of Agriculture No M. macrocicatrices in collection Georgia University of Georgia No M. macrocicatrices in collection Purdue University No M. macrocicatrices in collection Kentucky University of Kentucky No M. macrocicatrices in collection Maine Maine Forest Service No M. macrocicatrices in collection Maryland Smithsonian National Museum of Natural History No M. macrocicatrices in collection Massachusetts University of Massachusetts No M. macrocicatrices in collection Michigan State University No M. macrocicatrices in collection Mississippi State University No M. macrocicatrices in collection Newfoundland Memorial University No M. macrocicatrices in collection New Hampshire University of New Hampshire No M. macrocicatrices in collection New York Cornell University No M. macrocicatrices in collection North Carolina North Carolina State University No M. macrocicatrices in collection Ohio Ohio State University No M. macrocicatrices in collection Ontario Canadian National Collection M. macrocicatrices type series as described by Richards (1960) coll. from Lynedoch, Denbigh, and GrifÞth (Ontario), and Fredericton (New Brunswick)Ñall on P. strobus Pennsylvania Penn State University No M. macrocicatrices in collection Quebec McGill University No M. macrocicatrices in collection Rhode Island RI Museum of Natural History No M. macrocicatrices in collection Rhode Island University of Rhode Island No M. macrocicatrices in collection South Carolina Clemson No M. macrocicatrices in collection Tennessee University of Tennessee No M. macrocicatrices in collection Vermont Department of Forests, Parks, and Recreation M. macrocicatrices.VTa coll. from Montpelier ( Co.) and St. Johnsbury (Caledonia Co.) associated with S. pinicola, and from Dummerston (Windham Co.)Ñall on P. strobus Virginia Virginia Tech University No M. macrocicatrices in collection West Virginia West Virginia University No M. macrocicatrices in collection University of Wisconsin No M. macrocicatrices in collection

a New state record for M. macrocicatrices.

United States, but did result in a new state record for this species has never been reported or collected from this species in Vermont (Table 3). the southeastern United States. It was previously Fungus Identification. Of the 120 symptomatic P. known only from Massachusetts, New Brunswick, strobus branches collected from Georgia, 91.7% had M. New Hampshire, Nova Scotia, Ontario, and Quebec. macrocicatrices, 15.8% had C. pinea cankers, the patho- The museum survey added Vermont to this list; 2) this gen implicated in P. strobus dieback in Maine, New scale species has never been reported with P. strobus Hampshire, and West Virginia, and only 2.5% had S. showing signs of dieback or mortality; 3) M. macroci- pinicola fungal mats. Fungi isolated from the wood catrices has not been associated previously with fungal surrounding M. macrocicatrices included potentially pathogens; and 4) M. macrocicatrices has never been pathogenic species in the genera Pestalotiopsis and documented living outside the epiphytic mats of its Phomopsis along with a number of saprophytic fungi symbiotic fungus, S. pinicola. including Aspergillus niger Van Tieghem, Chaeto- The most recent detailed work regarding M. macro- phoma spp., and Peyronellaea spp. Of the different cicatrices was conducted by Watson et al. (1960) in the media used, 12.5% of the PNA plates contained Pesta- Canadian Maritimes where M. macrocicatrices was lotiopsis, 4.2% of the NashÐSnyder plates had Pestalo- found to be closely associated with S. pinicola, an tiopsis and 8.3% with Phomopsis, and 12.5% of the epiphytic, nonpathogenic, and mutualistic basidiomy- PDAϩSϩT plates contained Pestalotiopsis and 4.2% cete fungus (Couch 1938). Adult females of M. macro- had Phomopsis. No cultures of Fusarium, Diplodia, or cicatrices emerge in late spring to early summer and Caliciopsis, the fungi previously found associated with move away from the fungal mats to produce their P. strobus cankers in Virginia, were isolated. However, ovisacs in cryptic locations, such as bark crevices or in the case of Caliciopsis, there is no known selective under lichens (Watson et al. 1960). In Georgia, adults medium for this genus, and the media used may not emerged in late winter to early spring and the few have been optimal for isolation. ovisacs found were in cankers and twig beetle (Co- leoptera: Curculionidae: Scolytinae) galleries. After hatching, the mobile yellowÐbrown crawlers (0.6Ð1.5 Discussion mm) move back to the S. pinicola fungal mats where We provide the Þrst documentation of the presence they insert their stylets into the bark and become of M. macrocicatrices in six states in the southeastern stationary to form the intermediate cyst stage. The United States. These results are important because 1) high proportion of branches with M. macrocicatrices December 2013 MECH ET AL.: REPORT OF M. macrocicatrices IN SOUTHEASTERN U.S. 2397 lacking S. pinicola (97.3%) in our study suggests that, Acknowledgments although S. pinicola requires an insect for nutrition We thank B. Barnes, C. Brissey, and K. Smoot (University (Couch 1938), M. macrocicatrices is likely able to sur- of Georgia) for Þeld and laboratory support. J. Sullivan vive without the presence of fungal mats. (Georgia Forestry Commission); M. Bohne and I. Munck Watson et al. (1960) observed that the cyst stage (U.S. Department of Agriculture Forest Service); K. Lom- remained within the fungus for two winters, suggest- bard (New Hampshire Division of Forests and Lands); B. ing that M. macrocicatrices has a 2-yr life cycle. Al- Heath (North Carolina Forest Service); and K. Carrington, B. though males were not found initially, suggesting that Kesecker, and J. Rose (West Virginia Department of Agri- culture) kindly sent us P. strobus samples. We are also thank- this species may be parthenogenetic (Watson et al. ful to G. Stanosz and D. Smith (University of Wisconsin), G. 1960), males have been described (Richards 1960). Hodges (Florida Department of Agriculture and Consumer Adult females are 3.6Ð4.0 mm, have fully developed Sciences), and D. Henk (Imperial College, ) antennae and legs when they emerge from the cyst for their assistance with identiÞcations. Thanks also to T. stage (Fig. 1C), and are wingless. Adult males of M. Edgerton (Virginia Department of Forestry) for producing macrocicatrices emerge from a cocoon made of waxy the scale distribution map. Many researchers at various mu- “ ” seums assisted with specimen retrievals including S. Alm threads secreted by the prepupa and are winged (University of Rhode Island), B. Blinn (North Carolina State (Richards 1960). The phenology of M. macrocicatrices University), C. Bartlett (University of ), S. Boucher in the southeastern United States is currently under (McGill University), D. Chandler (University of New Hamp- investigation. However, the lack of overlapping gen- shire), T. Chapman (Memorial University), S. Clutts (Uni- erations and synchronous adult emergences in early versity of Kentucky), E. Day (Virginia Tech University), A. 2012 and again in early 2013 suggests that M. macro- Deans (Penn State University), J. Dombroskie (Cornell Uni- versity), C. Donahue (Maine Forest Service), F. Drummond cicatrices may have a 1-yr life cycle in Georgia. (University of Maine), R. Foottit (Canadian National Col- At present, we are unsure whether M. macrocica- lection), H. Ginsberg (Rhode Island Museum of Natural trices has always been present in the southeastern History), T. Hanson (Vermont Department of Forests, Parks, United States, but has been overlooked because of its and Recreation), R. Hoebeke (University of Georgia), S. small size and cryptic nature, or whether our Þndings Krauth (University of Wisconsin), P. Lambdin (University of reßect a relatively recent range expansion or intro- Tennessee), D. Miller (Smithsonian), J. Morse (Clemson University), L. Musetti (Ohio State University), B. Normark duction into these states. The absence of M. macroci- (University of Massachusetts), J. OÕDonnell (University of catrices in museum holdings from the southeastern Connecticut), G. Parsons (Michigan State University), A. United States supports the latter hypothesis (Table 3). Provonsha (Purdue University), C. Ray, Jr. (Auburn Univer- Conversely, S. pinicola was collected in North Caro- sity), T. Schiefer (Mississippi State University), I. Stocks lina in 1931 (Couch 1938) supporting the hypothesis (Florida Department of Agriculture), and J. Strazanac (West that M. macrocicatrices may have always been in the Virginia University). We thank the editor and two anony- mous reviewers for their constructive comments on this man- southeastern United States. More surveys in the native uscript. Funding was provided by the Daniel B. Warnell range of P. strobus will provide a better understanding School of Forestry and Natural Resources, University of of the distribution of M. macrocicatrices in North Georgia; U.S. Department of AgricultureÐForest Service, America. Forest Health Protection; and Virginia Department of For- Unlike some of the other pine bast scales, M. macro- estry. cicatrices has not historically been associated with tree dieback or mortality, which raises interesting ques- tions about its presence on symptomatic P. strobus, References Cited both in the southeastern United States and in its pre- Bean, J. L., and P. A. Godwin. 1955. Description and bion- viously documented range (New Hampshire). The omics of a new red pine scale Matsucoccus resinosae. For. variability of fungi found with cankers and tissue as- Sci. 1: 164Ð176. sociated with feeding individuals of M. macrocicatrices Bean, J. L., and P. A. Godwin. 1971. Red pine scale. U.S. Department of Agriculture Forest Service, Forest Insect in this and other investigations (Cram et al. 2009) and Disease Leaßet No. 10. (http://www.fs.usda.gov/ indicates that the insect is most likely not associated Internet/FSE_DOCUMENTS/fsbdev2_043074.pdf). with a single pathogen. Because scales are found either Benny, G. L., D. A. Samuelson, and J. W. Kimbrough. 1985. deeply embedded in the cankers or present on top of Studies in the Coryneliales. IV. Caliciopsis, Coryneliopsis the bark with clear necrotic tissue under their feeding and Coyneliospora. Bot. Gaz. 146: 437Ð448. area (Fig. 1B and D), we hypothesize that they may be Ben–Dov, Y. 2005. A systematic catalogue of the family (Hemiptera: Coccoidea) of the creating wounds that are then infested by opportu- world. Intercept Ltd., Wimborne, United Kingdom. nistic fungi such as C. pinea. The relative contributions Ben–Dov, Y. 2012. ScaleNet, Matsucoccus. (http://scalenet. of the scale insectÐfungal pathogen complex to canker info/validname/matsucoccus/). formation and tree dieback, and their interactions Biomatters. 2012. Geneious R6. (http://www.geneious. with each other, are also being investigated. Overall, com/). our study suggests that a closer examination of M. Blodgett, J. T., P. Bonello, and G. R. Stanosz. 2003. An ef- fective medium for isolating Sphaeropsis sapinea from macrocicatrices and associated pathogens may be war- asymptomatic . For. Pathol. 33: 395Ð404. ranted for the future health of natural and planted P. Booth, J. M., and P. J. Gullan. 2006. Synonymy of three strobus stands in North America. pestiferous Matsucoccus scale insects (Hemiptera: Coc- 2398 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 6

coidea: Matsucoccidae) based on morphological and mo- McClure, M. S. 1983. Population dynamics of a pernicious lecular evidence. Proc. Entomol. Soc. Wash. 108: 749Ð760. parasite: density-dependent vitality of red pine scale. Butler, B. J., R. S. Morin, and M. D. Nelson. 2012a. Massa- Ecology 64: 710Ð718. chusettsÕ forest resources, 2011. Res. Note NRS-150. U.S. Morin, R. S., and C. W. Woodall. 2012. New HampshireÕs Department of Agriculture Forest Service, Northern Re- forest resources, 2011. Res. Note. NRS-140. U.S. Depart- search Station, Newtown Square, PA. ment of Agriculture Forest Service, Northern Research Butler, B. J., R. S. Morin, and M. D. Nelson. 2012b. Rhode Station, Newtown Square, PA. IslandÕs forest resources, 2011. Res. Note. NRS-151. U.S. Morrison, H. 1939. Descriptions of new species of Matsu- Department of Agriculture Forest Service, Northern Re- coccus (Hemiptera: Coccidae). Proc. Entomol. Soc. search Station, Newtown Square, PA. Wash. 41: 1Ð20. Couch, J. N. 1938. The genus Septobasidium. University of Nelson, P. E., T. A. Toussoun, and W.F.O. Marasas. 1983. North Carolina Press, Chapel Hill, NC. Fusarium species: an illustrated manual for identiÞcation. Cram, M. M., C. Asaro, and T. Edgerton. 2009. Field inoc- Pennsylvania State University Press, University Park, PA. New Hampshire Division of Forests and Lands. 2012. Pest ulations of Caliciopsis pinea and Diplodia scrobiculata on alert. Red pine scale: Matsucoccus resinosae. (http:// eastern white pine, p. 13. In Proceedings, Southwide For- www.nhstateparks.org/uploads/pdf/RP_pestalert.pdf). est Disease Workshop, 29 JuneÐ2 July 2009, Greenville, Parr, T. J. 1939. Matsucoccus sp., a scale insect injurious to SC. U.S. Department of Agriculture Forest Service, For- certain pines in the northeast (Hemiptera-Homoptera). est Health Protection, Asheville, NC. J. Econ. Entomol. 32: 624Ð630. Dowton, M., and A. D. Austin. 1998. Phylogenetic relation- Rambaut, A. 2002. Se-Al sequence alignment editor, version ships among the microgastroid wasps (Hymenoptera: 2.0a11. (http://tree.bio.ed.ac.uk/software/seal/). Braconidae): combined analysis of 16S and 28S rDNA Ray, C. H., and M. L. Williams. 1991. Two new species of genes and morphological data. Mol. Phylogenet. Evol. 10: Matsucoccus Cockerell (Homoptera: Margarodidae) sim- 354Ð366. ilar to Matsucoccus alabamae Morrison. Proc. Entomol. Drooz, A. T. 1985. Insects of eastern forests. U.S. Depart- Soc. Wash. 93: 186Ð192. ment of Agriculture Forest Service, Miscellaneous Pub- Richards, W. R. 1960. A new species of Matsucoccus Cock- lication 1426, Washington, DC. erell (Homoptera: Coccoidea). Can. Entomol. 92: 179Ð Foldi, I. 2004. The Matsucoccidae in the Mediterranean ba- 181. sin with a world list of species (Hemiptera: Sternorrhyn- Rose, J. 2011. A decline in stateÕs white pine found. West cha: Coccoidea). Ann. Soc. Entomol. Fr. 40: 145Ð165. Virginia Department of Agriculture, Plant Industries Di- Kosztarab, M. 1996. Scale insects of northeastern North vision, Charleston, WV. America. IdentiÞcation, biology, and distribution. Vir- Steiner, G. W., and R. D. Watson. 1965. Use of surfactants ginia Museum of Natural History, Martinsburg, VA. in the soil dilution and plate count method. Phytopathol- Li, S. J., and H. B. Zhao. 1997. Study on selection of geo- ogy 55: 728Ð730. graphical provenances of Pinus tabulaeformis resistant to U.S. Department of Agriculture Forest Service, Forest Matsucoccus matsumurae Kuwana. Sci. Silvae Sin. 33: 307Ð Health Protection. 2013. Red pine scale: Matsucoccus 320. resinosae (Kuwana). (http://www.fs.fed.us/nrs/tools/ Llewellyn, J. 2013. White pine decline. (http://www. afpe/maps/pdf/RPS.pdf). isaontario.com/content/white-pine-decline). Von Dohlen, C. D., and N. A. Moran. 1995. Molecular phy- Lombard, K. 2003. Caliciopsis canker (pine canker): Ca- logeny of the Homoptera: a paraphyletic taxon. J. Mol. liciopsis pinea. (http://extension.unh.edu/resources/ Evol. 41: 211Ð223. Watson, W. Y., G. R. Underwood., and J. Reid. 1960. Notes Þles/Resource000999_Rep1148.pdf). on Matsucoccus macrocicatrices Richards (Homoptera: Maine Forest Service. 2008. Forest and shade tree insect Margarodidae) and its association with Septobasidium and disease conditions for Maine: a summary of the 2007 pinicola Snell in eastern Canada. Can. Entomol. 92: 662Ð situation. Summary Report No. 19. Forest Health and 667. Monitoring Division, Augusta, ME. Wendel, G. W., and H. C. Smith. 1990. Pinus strobus L. Martineau, R. 1964. Forest insect conditions: [in the prov- eastern white pine, pp. 476Ð488. In R. M. Burns and B. H. ince of Quebec]. Annual report of the forest insect and Honkala (eds.), Silvics of North America, vol. 1. . disease survey. Canadian Forest Service, Quebec, Can- Department of Agriculture Forest Service, Washington, ada. DC. McCambridge, W. F., and D. A. Pierce. 1964. Matsucoccus Whiting. M. F., J. C. Carpenter, Q. D. Wheeler, and W. C. acalyptus (Homoptera, Coccoidea, Margarodidae). Ann. Wheeler. 1997. The Strepsiptera problem: phylogeny of Entomol. Soc. Am. 57: 197Ð200. the holometabolous insect orders inferred from 18S and McCaskill, G. L., and W. H. McWilliams. 2012. MaineÕs for- 28S ribosomal DNA sequences and morphology. Syst. est resources, 2011. Res. Note. NRS-143. U.S. Department Biol. 46: 1Ð68. of Agriculture Forest Service, Northern Research Station, Newtown Square, PA. Received 27 May 2013; accepted 11 August 2013.